International Journal (2019) 30:1925–1932 https://doi.org/10.1007/s00192-018-03859-9

ORIGINAL ARTICLE

An epidemiologic study of pelvic organ in rural Chinese women: a population-based sample in China

Zhiyi Li1 & Tao Xu2 & Zhaoai Li3 & Jian Gong4 & Qing Liu5 & Lan Zhu1

Received: 19 October 2018 /Accepted: 18 December 2018 /Published online: 26 January 2019 # The International Urogynecological Association 2019

Abstract Introduction and hypothesis We aimed to investigate the prevalence and risk factors of symptomatic (POP) in rural China. Methods A cross-sectional study of POP was conducted in rural China from February 2014 to March 2016. In total, 25,864 rural women were recruited. All were asked to complete a questionnaire that included questions about their age, job, parity, diseases, and so on. Symptomatic POP was assessed using Pelvic Organ Prolapse Quantification (POP-Q) system staging and validation questionnaires. Multivariate logistic regression was used to assess the factors associated with symptomatic POP. Results The prevalence of symptomatic POP was 9.10%. There was a consistent trend toward an increasing prevalence of POP with increasing age, ranging from 2.53 to 13.40% (P < 0.0001). Women aged 50–59 years [adjusted odds ratio (AOR) 1.86, 95% confidence interval (CI) 1.46–2.37] were more likely to have POP than women aged 20–29 years. POP was positively associated with giving birth to more than three children (AOR 2.18, 95% CI 1.88–2.43). Cesarean section was a significant protective factor (AOR = 0.34, 95% CI 0.33-0.49) compared with vaginal delivery. Multivariate logistic re- gression analysis showed that obesity, constipation, smoking, coughing, gynecological diseases, and other physical dis- eases were also associated with POP. Conclusions Symptomatic POP affects a substantial proportion of women in rural China. Older age, multiparity, vaginal delivery, obesity, and many chronic conditions significantly increased the odds of developing symptomatic POP. Additional healthcare campaigns are needed to educate women in rural areas about POP.

Keywords Epidemiology . Pelvic organ prolapse . Prevalence . Risk factors . Rural

Abbreviations POP Pelvic organ prolapse * Lan Zhu POP-Q Pelvic Organ Prolapse Quantification [email protected] AOR Adjusted odds ratio 1 Department of Obstetrics and Gynecology, Peking Union Medical CIs Confidence intervals College Hospital, Peking Union Medical College, Chinese Academy BMI Body mass index of Medical Sciences, No. 1 ShuaiFu Road, Dongcheng District, Beijing, People’sRepublicofChina 2 Department of Epidemiology and Statistics, Institute of Basic Medical Sciences, Chinese Academy of Medical Sciences and Introduction School of Basic Medicine, Peking Union Medical College, Beijing, People’sRepublicofChina Pelvic organ prolapse (POP) is defined as the descent into or 3 Department of Gynecology and Obstetrics, Children’s Hospital of Shanxi Province, Shanxi, People’s Republic of China out of the of the pelvic organs, including the and the anterior and posterior vaginal walls. POP mainly results 4 Department of Gynecology and Obstetrics, Maternal and Child Health Hospital of Wuxi, Jiangsu, People’sRepublicofChina from dysfunction of support. POP is a common condition, and the prevalence has been increasing in recent 5 Department of Gynecology and Obstetrics, Maternal and Child Health Hospital of Gansu Province, Lanzhou, People’s Republic of decades. The prevalence reported in the literature varies great- China ly [1–5]. In addition, many women with stage 2 prolapse do 1926 Int Urogynecol J (2019) 30:1925–1932 not experience symptoms related to the prolapse. The exact control, with a uniform protocol, standardized methodology, state of prolapse can be defined by combining prolapse symp- and staff training program. The gynecologist who performed toms and the Pelvic Organ Prolapse Quantification (POP-Q) the physical examination and survey workers who collected stage. Although the prevalence of POP varies among different and recorded data were not allowed to participate in the study studies depending on the definition of POP and research meth- until they had undergone training and passed an examination. odology used, it is the most prevalent in low- and middle- income countries. In China, where the rural population con- stitutes nearly 50% of the total, representing ~605,990,000 Study instrument and data collection people, urban–rural health disparities are expected to be even more pronounced, since the central and local governments Patients answered sociodemographic questions and self- implement policies that favor urban areas [6]. In addition, in reported their height and weight; the medical staff asked par- rural areas, high fertility rates and more engagement in phys- ticipants questions about their previous health history data, ical labor are common. However, there are no epidemiological obstetric history, occupation, and presence or absence of con- studies regarding the incidence or prevalence of POP in rural stipation, chronic cough, smoking, alcohol consumption, and areas in China. Therefore, it is essential to conduct a study to reproductive and other health-related risk factors. A chronic investigate its prevalence and identify the potential cough was defined as one lasting >3 weeks. Constipation was sociodemographic risk factors. The aim of this study was to defined as having to strain to have a bowel movement for at evaluate the prevalence and risk factors of POP based on least 1 year [8]. Smoking was defined as those who smoked at symptoms and POP-Q stage among women in rural China. least once per month. In addition, current alcohol consump- tion was defined as the consumption of one or more alcoholic drink per month. The diseases included on the questionnaire Methods were diabetes, hypertension, and depression, which women were considered to if they reported having been diagnosed Study setting by a healthcare provider within the past 3 years. The gyneco- logical diseases included on the questionnaire were myoma, This was part of a nationwide, population-based, multistage, pelvic inflammatory disease, chronic pelvic , and endo- stratified study of female pelvic organ disorders in rural metriosis. Regarding the different delivery methods: If the Chinese women. The study represents an analysis of a subset same participant had undergone cesarean section (CS) and of data from that cross-sectional study. Detailed descriptions spontaneous vaginal delivery, we defined the delivery method of the recruitment process, sampling technique, and data col- as spontaneous vaginal delivery. If a patient experienced spon- lection protocols have been described previously [7]. The taneous vaginal delivery and assisted vaginal delivery in suc- sampling framework was constructed with six provinces ran- cessive pregnancies, we defined the delivery method as domly selected by computer-generated random numbers from assisted vaginal delivery. the six major geographic regions of mainland China. The fol- All participants were asked to complete a questionnaire that lowing six regions were included: northwest China, southwest consisted of eight symptoms, which was the short form of the China, north China, east China, northeast China, and south Pelvic Floor Distress Inventory-20 (PFDI-20). The Chinese China. According to the predetermined sample size, which version was already validated in a Chinese population [9]. was stratified by levels of economic development, three Each question had yes/no answers listed. If any participant counties were randomly selected from each province. Our responded positively to any of the eight questions, she re- target population consisted of all eligible residents aged 20– ceived a physical examination in the dorsal lithotomy posi- 99 years according to the updated census lists from the com- tion. The symptom questionnaire items are listed in Table 1. munity registry offices. In addition, the included participants All points except total vaginal length (TVL) were recorded must have lived in the area in which they were registered for at while the participant exerted maximum Valsalva effort. least 10 years prior to the study. Pregnant women and women Methods, definitions, and descriptions used conformed to who had undergone treatment for pelvic floor disorders were the standards recommended by the International Continence excluded from our study. The eligibility participants were Society (ICS). For each participant, we defined prolapse stage women aged 20-99 years and were recruited from February using the most advanced prolapse site. 2014 to March 2016. Eligible women in these counties were The dependent variable used in this study was the presence contacted and invited to participate in the survey. Approval of symptomatic POP. The definition of symptomatic POP was was obtained from the Research Ethical Committee of the an affirmative response to any of the eight questions and pres- Peking Union Medical College Hospital. Written consent ence of stage ≥2 POP upon a physical examination in the was obtained from all eligible participants. This survey was dorsal lithotomy position. Descriptive statistics were used to conducted under the guidance of the subcommittee for quality present data in tables and graphs. Int Urogynecol J (2019) 30:1925–1932 1927

Table 1 Eight prolapse symptoms

Symptom Question

Symptom 1 Do you usually experience heaviness or dullness in the pelvic area? Symptom 2 Do you usually have a bulge or something falling out that you can see or feel in your vaginal area? Symptom 3 Do you ever have to push on the vagina or around the rectum to have or complete a bowel movement? Symptom 4 Do you usually experience a feeling of incomplete bladder emptying? Symptom 5 Do you ever have to push up on a bulge in the vaginal area with your fingers to start or complete urination? Symptom 6 Do you usually feel any vaginal friction when you walk? Symptom 7 Do you usually experience urine leakage related to coughing, sneezing, or laughing? Symptom 8 Do you usually experience urine leakage associated with a feeling of urgency?

Statistical analysis body mass index (BMI) was 23.02 ± 3.12 kg/m2.The sociodemographic characteristics are presented in Table 2. All analyses were performed using SAS. Univariate and mul- Overall, 747 participants (3.01%) were minorities. The per- tivariate analyses were performed using chi-square tests and centages of participants that engaged in physical or mental binary logistic regression. Only variables that were significant labor were 85.34 and 14.66%, respectively; 88.50% were par- in univariate analyses and had been identified in previous ous, and 22.40% had three or more children. Regarding the studies as being either associated with POP or a potential type of delivery, 73.85% had experienced vaginal spontane- confounder of an association were included in the multivariate ous delivery, 13.86% had undergone a CS, and 0.79% had logistic regression model. All statistical tests were two sided, experienced vaginal-assisted deliveries. Prior pelvic and a P value <0.05 was considered statistically significant. In was reported by 7420 (29.86%) women; 3820 (15.37%) had addition, odds ratios (ORs) and 95% confidence intervals (CI) a coexisting disease, and 6998 (28.16%) had a gynecological of the variables that were considered possible risk factors were disease. Smoking was reported by 142 participants (0.57%), calculated in relation to the prolapse stages. and alcohol consumption by 869 (3.50%).

Results Prevalence of symptomatic POP The overall prevalence of POP in rural China was 9.23% Characteristics of the sample population (Table 3). Prolapse stage 2 accounted for 7.55%, stage 3 for 1.52%, and stage 4 0.16%. The incidence of POP increased Of the 54,993 participants, 25,864 were from rural areas. As with increasing age. The prevalence of each potential risk shown in Fig. 1, 24,848 were included in our data analysis. factor are depicted in Table 4. Women aged 50-59 years had The mean age of the women included in the final analysis was the highest incidence of POP (13.40%). Table 4 depicts the 45.40 ± 15.77 (standard deviation, SD) years, and the mean prevalence of symptomatic POP in all participants. POP was significantlymorecommoninwomenwhounderwent vaginal-assisted delivery (17.26%) than those who experi- Target enced spontaneous vaginal delivery (11.70%) and CS population 25864 (2.90%). The type of job also affected the prevalence of Excluded POP symptoms, which were more prevalent among women Age missing: 387 who performed physical labor (9.98%) than among those who Race missing: 228 performed mental labor (4.86%). Symptomatic POP was more Parity missing: 200 prevalent in women who had a chronic cough for at least Delivery pattern missing: 201 3 weeks (24.84%), were smokers (19.72%), had gynecologi- cal disease (14.52%), and had suffered constipation for at least 1 year (20.84%) compared with their counterparts with the corresponding negative traits. Multiparous, obese, and women Eligible for final analysis 24848 with a history of gynecological disease were more likely to have symptomatic POP (14.73%, 13.31%, and 14.52%, re- Fig. 1 Study flowchart spectively) than their counterparts with the opposite traits. 1928 Int Urogynecol J (2019) 30:1925–1932

Table 2 General characteristics of participants. Data are given as mean Factors associated with symptomatic POP ± standard deviation (SD) and number (%)

Characteristics Data Variables that had P values <0.05 in univariate analysis were included in the multivariate regression model. The results Age (years), mean (SD) 45.40 ± 15.77 showed that age, BMI, parity, constipation, smoking, cough, 20–29 4902 (19.73) gynecological diseases, and other diseases were independent 30–39 5385 (21.67) risk factors of POP (Table 4). Women aged 60-69 years (AOR 40–49 5524 (22.23) 2.19, 95% CI 1.72–2.79) were more likely to have POP than 50–59 3918 (15.77) women aged 20-29 years. Compared with women of normal 60–69 2595 (10.44) weight, overweight and obese women were more likely to ≥ 70 2524 (10.16) have POP (AOR = 1.2, 95% CI 1.09–1.33; AOR = 1.30, Body mass index (kg/m2), mean (SD) 23.02 ± 3.12 95% CI 1.11–1.53). Underweight (<18.5) 1386 (5.58) Women who had gynecological or other diseases were Normal (18.5–23.9) 14,821 (59.65) more likely to have POP (AOR = 1.324, 95% CI 1.173– Overweight (24–27.9) 7033 (28.30) 1.492, AOR = 2.08 95% CI 1.890-2.289, respectively) than Obese (≥28) 1608 (6.47) women who did not have concomitant illnesses. Smoking, Race coughing, and constipation were all risk factors for symptom- Han 24,101 (96.99) atic POP (AOR = 1.88, 95% CI 1.57-2.24; AOR = 1.64,95% Minority 747 (3.01) CI 1.04-2.51; AOR = 2.12,95% CI 1.86-2.41, respectively). Job Multivariate logistic regression analysis showed that Mental labor 3642 (14.66) nulliparity was a protective factor against symptomatic POP Physical labor 21,206 (85.34) (AOR = 0.119 95% CI 0.06-0.22). Regarding delivery pattern, Parity CS was also a significant protective factor (AOR = 0.335 95% Nulliparous 2857 (11.50) CI 0.33-0.49) compared with vaginal delivery. Primiparous (=1) 9173 (36.92) Multiparous (=2) 725 (129.01) Multiparous (≥3) 5567 (22.40) Discussion Delivery pattern Nulliparous 2857 (11.50) Epidemiological studies of symptomatic POP are rare in Vaginal spontaneous delivery 18,351 (73.85) China, especially in rural areas. This is one of the few Vaginal assisted delivery 197 (0.79) village-based studies using symptoms and physical examina- Cesarean section 3443 (13.86) tions to determine the prevalence of and risk factors for symp- Gynecological disease 6998 (28.16) tomatic POP. POP was identified in 30-70% of women pre- Other disease 3820 (15.37) senting for routine gynecologic examinations, but only 3–6% Smoking 142 (0.57) of those had descent beyond the hymen [10–12]. In the United Alcohol consumption 869 (3.50) States National Health and Nutrition Examination Survey Cough (>3 weeks) 851 (3.42) (NHANES), overall, 2.9% of women experienced symptom- Constipation (>1 year) 1876 (7.55) atic POP [13]. The prevalence of POP was 15.6% in a rural Pelvic surgery 7420 (28.86) Bangladeshi study [14]. The different prevalences in those Spinal surgery 80 (0.32) studies may be the result of the different definitions of POP adopted. The definition used in the NHANES and Other diseases included diabetes, hypertension, and depression; gyneco- logical diseases included myoma, pelvic inflammatory disease, chronic Bangladeshi study was a positive response to the question: , and BDo you experience bulging or an object falling out that you SD standard deviation can see or feel in the vaginal area?^ There was no physical examination performed to confirm the prolapse. This is

Table 3 Prevalence of each prolapse stage. Data are given as No symptomatic POP or POP stage 1 Symptomatic POP number (%) POP stage 2 POP stage 3 POP stage 4

22,555 (90.77%) 1875 (7.55) 378 (1.52%) 40 (0.16%)

POP pelvic organ prolapse Int Urogynecol J (2019) 30:1925–1932 1929

Table 4 Weighted logistic regression for predictors of pelvic organ prolapse (POP). Data are given as number (%) and odds ratios (OR) [95% confidence intervals (CI)]

Independent variables Symptomatic POP Symptomatic POP (unadjusted) Symptomatic POP (adjusted)

N (%) OR 95% CI P value OR 95% CI P value

Age 20–29 (ref) 124 (2.53) 30–39 341 (6.33) 2.61 2.12–3.22 <0.001 1.18 0.95–1.48 0.06 40–49 707 (12.80) 5.66 4.67–6.90 <0.001 1.75 1.42–2.17 <0.001 50–59 525 (13.40) 5.96 4.90–7.32 <0.001 1.86 1.46–2.37 <0.001 60–69 320 (12.33) 5.42 4.32–6.73 <0.001 1.59 1.21–2.10 <0.001 ≥ 70 276 (10.94) 4.73 3.82–5.90 <0.001 1.27 0.94–1.69 0.0676 BMI (kg/m2) Normal (18.5–23.9) (ref) 1187 (8.01) Underweight (<18.5) 73 (5.27) 0.64 0.50-0.82 <0.001 0.80 0.62–1.03 Overweight (24–27.9) 819 (11.65) 1.51 1.38–1.66 <0.001 1.21 1.09–1.33 <0.001 Obese (≥28) 214 (13.31) 1.76 1.51-2.06 <0.001 1.37 1.16–1.61 <0.001 Parity <0.001 Primiparous (=1) (ref) 607 (6.62) Nulliparous 12 (0.42) 0.06 0.03–0.10 <0.001 0.12 0.06–0.22 <0.001 Multiparous (=2) 854 (11.78) 1.88 1.69–2.10 <0.001 1.60 1.42–1.80 <0.001 Multiparous (≥3) 820 (14.73) 2.44 2.83–2.72 <0.001 2.18 1.88–2.43 <0.001 Delivery pattern Vaginal spontaneous delivery (ref) 2147 (11.70) Vaginal assisted delivery 34 (17.26) 1.55 1.07–2.25 <0.001 1.66 1.54–2.62 <0.001 Cesarean section 100 (2.90) 0.23 0.18–0.28 <0.001 0.34 0.33-0.49 <0.001 Job <0.001 0.10 Physical labor (ref) 2116 (9.98) Mental labor 177 (4.86) 0.46 0.39–0.54 0.96 0.81–1.15 0.08 Race 0.068 – Han 2237 (9.28) Minority 56 (7.50) 0.79 0.60–1.03 –– – Smoking <0.001 <0.001 No (ref) 2265 (9.17) Yes 28 (19.72) 2.43 1.58–3.63 1.88 1.57–2.24 Alcohol consumption <0.001 <0.001 No (ref) 2187 (9.12) Yes 106 (12.20) 1.35 1.13–1.62 1.09 1.01–1.14 Cough (>3 weeks) <0.001 <0.001 No (ref) 2083 (8.68) Yes 210 (24.68) 3.45 2.93–4.05 1.64 1.04–2.51 Constipation (>1 year) <0.001 <0.001 No (ref) 1902 (8.28) Yes 391 (20.84) 2.92 2.58–3.29 2.12 1.86–2.41 Gynecological disease <0.001 <0.001 No (ref) 1277 (7.15) Yes 1016 (14.52) 2.20 2.012–2.41 2.08 1.89–2.29 Other disease <0.001 <0.001 No (ref) 1685 (8.01) Yes 608 (15.92) 2.17 1.97–2.40 1.32 1.17–1.49 Pelvic surgery 0.12 – 1930 Int Urogynecol J (2019) 30:1925–1932

Table 4 (continued)

Independent variables Symptomatic POP Symptomatic POP (unadjusted) Symptomatic POP (adjusted)

N (%) OR 95% CI P value OR 95% CI P value

No (ref) 1647 (9.45) Yes 646 (8.71) 0.99 0.86–1.012 –– Spine surgery 0.15 – No (ref) 2290 (9.25) Yes 3 (3.75) 0.49 0.20–1.33 ––

Other diseases included diabetes, hypertension, and depression; Gynecological disease included myoma, pelvic inflammatory disease, chronic pelvic pain, and endometriosis. Variables were included in the multivariate analysis if they exhibited a significant association in the univariate analysis (P < 0.05) or were identified in previous studies as being associated with POP. Race, pelvic surgery, and spinal surgery were not included in the model, as these factors were not statistically significant in the univariate logistic regression analyses BMI body mass index different from our definition, which was based on both symp- with those who were not multiparous [18, 23]. Given the large toms and POP-Q stage. Apart from this, differences in the rural population and increased number of deliveries by rural prevalence may have also resulted from the population in- Chinese women, interventions targeting these risk factors to volved in studies and the socioeconomic growth. There is prevent POP are needed. more expenditure on public health in developed countries than Multivariate results indicated that smoking and coughing in developing and undeveloped countries. Therefore, the prev- can also exacerbate POP, as they increase intra-abdominal alence of POP in developed countries such as the USA is pressure, risk of POP 1.63-fold (95% CI 1.04–2.50), and much lower than in developing and undeveloped countries. 1.86-fold (95% CI 1.55–2.22), respectively. Constipation According to the same study conducted in urban China was also found to be associated with POP, which is consistent (manuscript being prepared), prevalence in the rural area with the results of a recent study conducted in the United Arab was lower than that in the urban area. We found that most Emirates [17]. Although constipation could be generated by patients with symptomatic POP in our study had stage 2 pro- POP, some studies have shown that straining to produce stool lapses. Urban women pay more attention to their quality of life as a young adult prior to the onset of POP was more common and are more sensitive to illness and discomfort, leading to a in women who subsequently developed POP than in women higher rate of self-perceived illness among urban women than who did not (61 vs 4%, P <0.001)[24]. More longitudinal among rural women [6, 15, 16]; rural women may neglect studies are required to explore the relationship between con- symptoms that do not seriously affect their daily lives. stipation and POP. However, all these characteristics have the Similarly, incidence rates of hypertension, diabetes, and other potential to be modified. Therefore, efforts should be strength- chronic diseases were higher among urban than rural resi- ened to improve access to family planning. Controlling weight dents, indicating that people in rural areas are reluctant to seek and avoiding a chronic cough and constipation can reduce the healthcare unless they are impaired by the health problems likelihood of developing symptomatic POP. Data are conflict- [15]. In addition, limited by their lower economic status, ing regarding whether the risk of prolapse is increased in the demand for healthcare among rural residents is not as women with certain occupations [25]. One study of >1000 high as among those living in urban areas. Therefore, the women reported that women who engage in manual labor different degree of attention to health in rural and urban have significantly more severe POP than women engaged in areas may cause the difference in the prevalence of POP. other jobs, likely as a result of increased intra-abdominal pres- Considering the reduced attention to health in rural areas, sure related to more heavy lifting and standing for long pe- we should strengthen health-related information and edu- riods [26]. In our analysis, there was no significant association cation in rural areas. between symptomatic POP and physical labor. More studies Several factors in our study were also associated with POP in the general population correlating jobs with the incidence of in previous studies, including multiparity, advanced age, and POP are needed. increased BMI [2, 17–21]. With increasing age, the preva- Strengths of this study include screening for symptomatic lence of symptomatic POP increases. Obese women had a POP based on both the presence of prolapse-related symptoms greater risk of POP than nonobese women in our study, which and POP-Q stage. Furthermore, our study includes a large was similar to results reported in a previous study [22]. representative population-based sample of rural women and Consistent with prior studies, being multiparous (parity ≥3) had a high response rate. This was the largest population- significantly increased the risk of symptomatic POP compared based epidemiologic study of POP in rural China. Our study Int Urogynecol J (2019) 30:1925–1932 1931 had some limitations: The prevalence of POP may be Urogynecol J. 2011;22(2):127–35. https://doi.org/10.1007/s00192- underestimated, because screening based on prolapse-related 010-1215-0. 4. Chow D, Rodriguez LV. Epidemiology and prevalence of pelvic symptoms may miss women without symptoms. In addition, organ prolapse. Curr Opin Urol. 2013;23(4):293–8. https://doi. the low level of attention to health in rural areas may result in org/10.1097/MOU.0b013e3283619ed0. an underestimated prevalence of POP. Another weakness is 5. Swift SE. The distribution of pelvic organ support in a population of that our study excluded who underwent treatment for pelvic female subjects seen for routine gynecologic health care. Am J Obstet Gynecol. 2000;183(2):277–85. floor disorders. 6. Li J, Shi L, Liang H, Ding G, Xu L. Urban-rural disparities in health This was the largest population-based epidemiological care utilization among Chinese adults from 1993 to 2011. BMC study to date to examine symptomatic POP in rural China. Health Serv Res. 2018;18(1):102. More than 9% of adult women in rural China experience 7. ZhangC,TongJ,ZhuL,ZhangL,XuT,LangJ,etal.A symptomatic POP. 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